The Journal of Neuroscience, April 22, 2009, 29(16):5062-5074; doi:10.1523/JNEUROSCI.0716-09.2009
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Cellular/Molecular
Complex Intrinsic Membrane Properties and Dopamine Shape Spiking Activity in a Motor Axon
Aleksander W. Ballo and
Dirk Bucher
The Whitney Laboratory for Marine Bioscience and Department of Neuroscience, University of Florida, St. Augustine, Florida 32080
Correspondence should be addressed to Dr. Dirk Bucher, The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd., St. Augustine, FL 32080. Email: bucher{at}whitney.ufl.edu
We studied the peripheral motor axons of the two pyloric dilator (PD) neurons of the stomatogastric ganglion in the lobster, Homarus americanus. Intracellular recordings from the motor nerve showed both fast and slow voltage- and activity-dependent dynamics. During rhythmic bursts, the PD axons displayed changes in spike amplitude and duration. Pharmacological experiments and the voltage dependence of these phenomena suggest that inactivation of sodium and A-type potassium channels are responsible. In addition, the "resting" membrane potential was dependent on ongoing spike or burst activity, with more hyperpolarized values when activity was strong. Nerve stimulations, pharmacological block and current clamp experiments suggest that this is due to a functional antagonism between a slow after-hyperpolarization (sAHP) and inward rectification through hyperpolarization-activated current (IH). Dopamine application resulted in modest depolarization and "ectopic" peripheral spike initiation in the absence of centrally generated activity. This effect was blocked by CsCl and ZD7288, consistent with a role of IH. High frequency nerve stimulation inhibited peripheral spike initiation for several seconds, presumably due to the sAHP. Both during normal bursting activity and antidromic nerve stimulation, the conduction delay over the length of the peripheral nerve changed in a complex manner. This suggests that axonal membrane dynamics can have a substantial effect on the temporal fidelity of spike patterns propagated from a spike initiation site to a synaptic target, and that neuromodulators can influence the extent to which spike patterns are modified.
Received Feb. 11, 2009;
revised March 12, 2009;
accepted March 17, 2009.
Correspondence should be addressed to Dr. Dirk Bucher, The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd., St. Augustine, FL 32080. Email: bucher{at}whitney.ufl.edu
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